Skip to main content
SpringerLink
Log in

Genome-Wide Identification and Expression Analysis of the Carotenoid Cleavage Oxygenase Gene Family in Five Rosaceae Species

  • Original Article
  • Published:
Plant Molecular Biology Reporter Aims and scope Submit manuscript

Abstract

The carotenoid cleavage oxygenases (CCOs), which include carotenoid cleavage dioxygenases (CCDs) and 9-cis-epoxycarotenoid dioxygenases (NCEDs), are enzymes that are critical to the mediation of the degradation of carotenoids to apocarotenoids. In this study, we identified a total of 12, 20, 11, 8, and 10 CCO genes from Pyrus bretschneideri, Malus domestica, Fragaria vesca, Prunus mume, and Prunus persica, respectively. Phylogenetic analysis showed that these CCO genes clustered into six groups (NCED, CCD1, CCD4, CCD7, CCD8, and CCD-like). Gene structure analysis revealed that CCO genes within the same groups showed similar exon numbers and contained similar motifs. Duplication analysis revealed that tandem duplication played a significant role in the expansion of CCO members in Malus domestica. Purifying selection was involved in the evolution of CCO genes in Pyrus bretschneideri. The transcriptomic data-based expression analysis revealed that the CCO genes exhibited distinct patterns of expression in the roots, leaves, buds, and fruit. The expression patterns based on qRT-PCR showed that there were greater differences on the relative expression levels of PbCCD1 and PbCCD5 between cultivars “Enli” (inflorescence sparsely branched) and “Jinxiangshui” (inflorescence copiously branched) in the three different stages of flower bud morphological differentiation, revealing the possibility of involvement of these genes in the branching of the pear inflorescence. This study provides a valuable resource for further investigations of CCO gene functions in Rosaceae species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Ahrazem O, Gómez-Gómez L, Rodrigo M, Avalos J, Limón M (2016) Carotenoid cleavage oxygenases from microbes and photosynthetic organisms: features and functions. Int J Mol Sci 17:1781

    Article  PubMed Central  CAS  Google Scholar 

  • An N, Fan S, Wang Y, Zhang L, Gao C, Zhang D, Han M (2018) Genome-wide identification, characterization and expression analysis of long non-coding RNAs in different tissues of apple. Gene 666:44–57

    Article  CAS  PubMed  Google Scholar 

  • Angela R, José Luís R, Marcella S, Dolores GM, Diego O, Antonio G, Lourdes GG (2008) Cytosolic and plastoglobule-targeted carotenoid dioxygenases from Crocus sativus are both involved in beta-ionone release. J Biol Chem 283:24816–24825

    Article  CAS  Google Scholar 

  • Auldridge M et al (2013) Characterization of three members of the Arabidopsis carotenoid cleavage dioxygenase family demonstrates the divergent roles of this multifunctional enzyme family. Plant J 2:G8–G10

    Google Scholar 

  • Bailey TL, Johnson J, Grant CE, Noble WS (2015) The MEME Suite. Nucleic Acids Res 43:W39-49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bao Z et al (2015) Disruption of a carotenoid cleavage dioxygenase 4 gene converts flower colour from white to yellow in Brassica species. New Phytol 206:1513–1526

    Article  CAS  Google Scholar 

  • Beveridge CA, Dun EA, Catherine R (2009) Pea has its tendrils in branching discoveries spanning a century from auxin to strigolactones. Plant Physiol 151:985–990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Biswas S, Akey JM (2006) Genomic insights into positive selection. Trends Genet 22:437–446

    Article  CAS  PubMed  Google Scholar 

  • Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL (2009) BLAST+: architecture and applications. BMC Bioinformatics 10:421

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13(1194):1202

    Google Scholar 

  • Chen H et al (2018) Genome-wide analysis of carotenoid cleavage oxygenase genes and their responses to various phytohormones and abiotic stresses in apple (Malus domestica). Plant Physiol Biochem 123:81–93

    Article  CAS  PubMed  Google Scholar 

  • Chernys JT, Zeevaart JA (2000) Characterization of the 9-cis-epoxycarotenoid dioxygenase gene family and the regulation of abscisic acid biosynthesis in avocado. Plant Physiol 124:343–353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Colaiacovo M et al (2012) A survey of microRNA length variants contributing to miRNome complexity in peach (Prunus Persica L.). Front Plant Sci 3:165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Colombo AR, Triche TJ Jr, Ramsingh G (2017) Arkas: rapid reproducible RNAseq analysis. F1000Res 6:586

    Article  PubMed  PubMed Central  Google Scholar 

  • Dun EA, Brewer PB, Beveridge CA (2009) Strigolactones: discovery of the elusive shoot branching hormone trends in plant. Science 14:364–372

    CAS  Google Scholar 

  • Dun EA, Germain ADS, Rameau C, Beveridge CA (2013) Dynamics of strigolactone function and shoot branching responses in Pisum sativum. Mol Plant 6:128–140

    Article  CAS  PubMed  Google Scholar 

  • Eddy SR (1998) Profile hidden Markov models;review. Bioinformatics 14:755

    Article  CAS  PubMed  Google Scholar 

  • Ferguson BJ, Beveridge CA (2009) Roles for auxin, cytokinin, and strigolactone in regulating shoot branching. Plant Physiol 149:1929–1944

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foster TM et al (2018) Expression of MdCCD7 in the scion determines the extent of sylleptic branching and the primary shoot growth rate of apple trees. J Exp Bot 69:2379–2390

    Article  CAS  PubMed  Google Scholar 

  • Hai-Feng J, Ye-Mao C, Chun-Li L, Dong L, Jing-Jing L, Ling Q, Yuan-Yue S (2011) Abscisic acid plays an important role in the regulation of strawberry fruit ripening. Plant Physiol 157:188–199

    Article  CAS  Google Scholar 

  • Harrison PJ, Bugg TDH (2014) Enzymology of the carotenoid cleavage dioxygenases: reaction mechanisms, inhibition and biochemical roles. Arch Biochem Biophys 544:105–111

    Article  CAS  PubMed  Google Scholar 

  • Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2014) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296

    Article  PubMed  PubMed Central  Google Scholar 

  • Jinfen Y, Zhenfei G (2007) Cloning of a 9-cis-epoxycarotenoid dioxygenase gene (SgNCED1) from Stylosanthes guianensis and its expression in response to abiotic stresses. Plant Cell Rep 26:1383–1390

    Article  CAS  Google Scholar 

  • Kloer D, Schulz G (2006) Structural and biological aspects of carotenoid cleavage. Cell Mol Life Sci CMLS 63:2291–2303

    Article  CAS  PubMed  Google Scholar 

  • Krzywinski M, Schein JI (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19:1639–1645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee TH, Tang H, Wang X, Paterson AH (2013) PGDD: a database of gene and genome duplication in plants. Nucleic Acids Res 41:D1152-1158

    Article  CAS  PubMed  Google Scholar 

  • Leng P, Yuan B, Guo Y (2014) The role of abscisic acid in fruit ripening and responses to abiotic stress. J Exp Bot 65:4577

    Article  CAS  PubMed  Google Scholar 

  • Letunic I, Doerks T, Bork P (2012) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res 40:D302-305

    Article  CAS  PubMed  Google Scholar 

  • Li X et al (2016) Genome-wide identification, evolution and functional divergence of MYB transcription factors in Chinese white pear (Pyrus bretschneideri). Plant Cell Physiol 57:824–847

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Ma J et al (2014) Inactivation of a gene encoding carotenoid cleavage dioxygenase (CCD4) leads to carotenoid-based yellow coloration of fruit flesh and leaf midvein in peach. Plant Mol Biol Report 32:246–257

    Article  CAS  Google Scholar 

  • Marasco EK, Schmidt-Dannert C (2008) Identification of bacterial carotenoid cleavage dioxygenase homologues that cleave the interphenyl alpha, beta double bond of stilbene derivatives via a monooxygenase reaction. Chem Bio Chem 9:1450–1461

    Article  CAS  PubMed  Google Scholar 

  • Mathieu S, Terrier N, Jm P, Bigey F, Günata Z (2005) A carotenoid cleavage dioxygenase from Vitis vinifera L.: functional characterization and expression during grape berry development in relation to C13-norisoprenoid accumulation. J Exp Bot 56:2721–2731

    Article  CAS  PubMed  Google Scholar 

  • Metsalu T, Vilo J (2015) ClustVis: a web tool for visualizing clustering of multivariate data using principal component analysis and heatmap. Nucleic Acids Res 43:W566-570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mikihisa U et al (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195–200

    Article  CAS  Google Scholar 

  • Nisar N, Li L, Lu S, Khin NC, Pogson BJ (2015) Carotenoid metabolism in plants. Mol Plant 8:68–82

    Article  CAS  PubMed  Google Scholar 

  • Ohmiya A (2009) Carotenoid cleavage dioxygenases and their apocarotenoid products in plants. Plant Biotechnol 26:351–358

    Article  CAS  Google Scholar 

  • Ohmiya A, Kishimoto S, Aida R, Yoshioka S, Sumitomo K (2006) Carotenoid cleavage dioxygenase (CmCCD4a) contributes to white color formation in chrysanthemum petals. Plant Physiol 142:1193–1201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rachele F et al (2013) Three distinct mutational mechanisms acting on a single gene underpin the origin of yellow flesh in peach. Plant J Cell Mol Biol 76:175–187

    Article  CAS  Google Scholar 

  • Ratnakar V, Bradbury LMT, Wurtzel ET (2010) The carotenoid dioxygenase gene family in maize, sorghum, and rice. Arch Biochem Biophys 504:104–111

    Article  CAS  Google Scholar 

  • Simkin AJ, Schwartz SH, Auldridge M, Taylor MG, Klee HJ (2004a) The tomato carotenoid cleavage dioxygenase 1 genes contribute to the formation of the flavor volatiles β-ionone, pseudoionone, and geranylacetone. Plant J 40:882–892

  • Simkin AJ et al (2004b) Circadian regulation of the PhCCD1 carotenoid cleavage dioxygenase controls emission of β-ionone, a fragrance volatile of petunia flowers. Plant Physiol 136:3504–3514

  • Singh VK, Mangalam AK, Dwivedi S, Naik S (1998) Primer premier: program for design of degenerate primers from a protein sequence. Biotechniques 24:318–319

    Article  CAS  PubMed  Google Scholar 

  • Sui X, Kiser PD, von Lintig J, Palczewski K (2013) Structural basis of carotenoid cleavage: from bacteria to mammals. Arch Biochem Biophys 539:203–213

    Article  CAS  PubMed  Google Scholar 

  • Surbanovski N, Brilli M, Moser M, Si-Ammour A (2016) A highly specific microRNA-mediated mechanism silences LTR retrotransposons of strawberry. Plant J 85:70–82

    Article  CAS  PubMed  Google Scholar 

  • Tan BC, Joseph LM, Deng WT, Liu L, Li QB, Cline K, McCarty DR (2003) Molecular characterization of the Arabidopsis 9-cis epoxycarotenoid dioxygenase gene family. Plant J 35:44–56

    Article  CAS  PubMed  Google Scholar 

  • Vallabhaneni R, Bradbury LM, Wurtzel ET (2010) The carotenoid dioxygenase gene family in maize, sorghum, and rice. Arch Biochem Biophys 504:104–111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Victoria GR et al (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194

    Article  CAS  Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  CAS  PubMed  Google Scholar 

  • Walter MH, Floss DS, Strack D (2010) Apocarotenoids: hormones, mycorrhizal metabolites and aroma volatiles. Planta 232:1–17

    Article  CAS  PubMed  Google Scholar 

  • Walter MH, Strack D (2011) Carotenoids and their cleavage products: biosynthesis and functions. Nat Prod Rep 28:663–692

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Ding G, Gu T, Ding J, Li Y (2017) Bioinformatic and expression analyses on carotenoid dioxygenase genes in fruit development and abiotic stress responses in Fragaria vesca. Mol Genet Genomics 292:895–907

    Article  CAS  PubMed  Google Scholar 

  • Wang Y et al (2012) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40:e49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei Y et al (2016) A comprehensive analysis of carotenoid cleavage dioxygenases genes in Solanum Lycopersicum. Plant Mol Biol Rep 34:512–523

    Article  CAS  Google Scholar 

  • Wilkins MR, Gasteiger E, Bairoch A, Sanchez JC, Williams KL, Appel RD, Hochstrasser DF (1999) Protein identification and analysis tools in the ExPASy server. Methods Mol Biol 112:531–552

    CAS  PubMed  Google Scholar 

  • Wu J et al (2013) The genome of the pear (Pyrus bretschneideri Rehd.). Genome Res 23:396–408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi T, Yamamoto K, Asano Y (2014) Identification and characterization of CYP79D16 and CYP71AN24 catalyzing the first and second steps in L-phenylalanine-derived cyanogenic glycoside biosynthesis in the Japanese apricot, Prunus mume Sieb. et Zucc. Plant Mol Biol 86:215–223

    Article  CAS  PubMed  Google Scholar 

  • Yu CS, Lin CJ, Hwang JK (2004) Predicting subcellular localization of proteins for Gram-negative bacteria by support vector machines based on n-peptide compositions. Protein Sci 13:1402–1406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J (2003) Evolution by gene duplication: an update. Trends Ecol Evol 18:292–298

    Article  Google Scholar 

Download references

Acknowledgements

We appreciate those contributors who make the transcriptome data accessible in public databases. We also thank International Science Editing (http://www.internationalscienceediting.com) for editing this manuscript.

Funding

This work was funded by the National Natural Science Foundation of China (no. 31301739) and Fundamental Research Funds for the Central Universities (KYZ201834).

Author information

Author notes

  1. Jianrong Zhao and Jiyu Li contributed equally to this work.

Authors and Affiliations

  1. College of Resource and Environment, Anhui Science and Technology University, Fengyang, 233100, People’s Republic of China

    Jianrong Zhao

  2. College of Horticulture, Nanjing Agricultural University, Nanjing, 210095, People’s Republic of China

    Jun Zhang, Dan Chen & Huping Zhang

  3. Horticultural Research Institute, Anhui Academy of Agricultural Sciences (Key Laboratory of Genetic Improvement and Ecophysiology of Horticultural Crop, Anhui Province), Hefei, 230001, People’s Republic of China

    Jiyu Li, Chunyan Liu & Gaihua Qin

  4. Key Laboratory of Fruit Quality and Developmental Biology, Anhui Academy of Agricultural Sciences, Hefei, 230001, People’s Republic of China

    Jiyu Li, Chunyan Liu & Gaihua Qin

Authors
  1. Jianrong Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jiyu Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jun Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dan Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Huping Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chunyan Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Gaihua Qin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Jiyu Li or Gaihua Qin.

Ethics declarations

Conflict of Interest

The authors declare no conflict of interest.

Additional information

Key Message

• A total of 12, 20, 11, 8, and 10 CCO genes were identified from Pyrus bretschneideri, Malus domestica, Fragaria vesca, Prunus mume, and Prunus persica, respectively.

• Tandem duplication played a significant role in the expansion of CCO members in Malus domestica.

• PbCCOs may play a role in the branching of pear inflorescences.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, J., Li, J., Zhang, J. et al. Genome-Wide Identification and Expression Analysis of the Carotenoid Cleavage Oxygenase Gene Family in Five Rosaceae Species. Plant Mol Biol Rep 39, 739–751 (2021). https://doi.org/10.1007/s11105-021-01284-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11105-021-01284-9

Keywords

Search

Navigation